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Isolation and Speciation of Tidepool Fishes As a Consequence of Quaternary Sea-Level Fluctuations

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Isolation and Speciation of Tidepool Fishes As a Consequence of Quaternary Sea-Level Fluctuations Isolation and speciation of tidepool fishes as a consequence of Quaternary sea-level fluctuations Raphael M. Macieira, Thiony Simon, Caio R. Pimentel & Jean-Christophe Joyeux Environmental Biology of Fishes ISSN 0378-1909 Volume 98 Number 1 Environ Biol Fish (2015) 98:385-393 DOI 10.1007/s10641-014-0269-0 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Environ Biol Fish (2015) 98:385–393 DOI 10.1007/s10641-014-0269-0 Isolation and speciation of tidepool fishes as a consequence of Quaternary sea-level fluctuations Raphael M. Macieira & Thiony Simon & Caio R. Pimentel & Jean-Christophe Joyeux Received: 18 October 2013 /Accepted: 28 April 2014 /Published online: 18 May 2014 # Springer Science+Business Media Dordrecht 2014 Abstract Dispersal is fundamental to the colonization of Introduction oceanic islands that were never connected to larger land- masses. For species with limited dispersal capabilities, Intertidal fishes comprise a group of species that live in a colonization of remote islands can be followed by isola- stressful and changing habitat where environmental char- tion and speciation. The tidepool fish community of acteristics and ecological processes act synergically toward Trindade Island, 1,160 km off the Brazilian coast at the structuring the community (Gibson 1986;Barlow1999; eastern end of the Vitória-Trindade Chain, is composed Horn et al. 1999). During the ebb tide, these fishes are of 18 species from 11 families. Four endemics generally concentrated in tidepools, where density and accounted for 48 % of the total number and 10 % of species composition are defined by intrinsic features such the total fish weight in tidepools. The fact that the five as exposure to waves (Gibson 1972; Grossman 1982), species confirmed to be endemic to Trindade are restrict- substrate cover (Bennett and Griffith 1984;Davis2000; ed to intertidal and shallow waters indicate that in the Arakaki and Tokeshi 2011), pool size (Mahon and Mahon present interglacial period the seamounts of the Vitória- 1994;Davis2000; Macieira and Joyeux 2011), depth Trindade Chain do not allow dispersal following a (Gibson 1972;Barton1982; Castellanos-Galindo et al. stepping-stones model. Thus, seamounts must have 2005; Cox et al. 2010) and habitat complexity (Davis been used as stepping-stones when emerged during 2000; Griffiths et al. 2006; Rojas and Ojeda 2010). One lower sea-level periods of the Pleistocene, but this con- of the most important, yet least studied, factors is the nection was definitively interrupted when they became nature of the substrate (e.g., carbonate, limestone, basalt) submerged at the end of the last glaciation. This high- where tidepools are located because its physical, chemical lights the importance of considering sea level fluctua- and mechanical properties (e.g., porosity, rugosity, sol- tions as a structuring factor of intertidal and shallow ubility, hardness, specific heat capacity, alkalinity) can water communities at oceanic localities. affect key features such as habitat complexity, substrate cover and water characteristics (Cox et al. 2010). Looking at the evolutionary history of the species Keywords Allopatric speciation . Intertidal fishes . inhabiting the intertidal zone can be a useful approach to Brazil . Endemic species . Lowstands . Stepping-stones understand community composition and structure be- cause habitat specialization, adaptation and dispersal R. M. Macieira (*) : T. Simon : C. R. Pimentel : ability are important traits on which the community J.<C. Joyeux is built (Prochazka et al. 1999; Rocha and Bowen Laboratório de Ictiologia, Departamento de Oceanografia e 2008). In conjunction, the attributes of each species Ecologia, Universidade Federal do Espírito Santo, 29075-910 Vitória, ES, Brazil will determine the community composition by filtering e-mail: [email protected] the occurrence of some species and permitting the Author's personal copy 386 Environ Biol Fish (2015) 98:385–393 presence of others. Intertidal fish communities gener- that Quaternary sea-level fluctuations shaped intertidal ally are dominated by resident species that have communities at certain oceanic localities. negative buoyancy (resulting from the absence or reduction of the swimbladder), small body size, reduced swimming performance (or saltated swim- Methods ming), cryptic behavior, and substrate-fixed spawning with parental care (Gibson 1986;Barlow1999; Study area DeMartini 1999;Zanderetal.1999). Their depen- dence upon tidepool habitats and, often, their re- Trindade Island (20°30′ S, 29°20′ W) and Martin Vaz duced ability for larval dispersal can limit the Archipelago (40 km farther east) are the extremity and chances of success in settlement events (Marliave only emerged parts of the Vitória-Trindade Chain. The 1977, 1986; Pfister 1999;Shanks2009; Salinas-de- chain is composed of a linear sequence of volcanic León et al. 2012), especially at remote oceanic islands seamounts whose summits are between 50 and 80 m where dispersal is fundamental in generating biodiver- deep (Fig. 1). Located 1,160 km off the coast, Trindade sity (Cowie and Holland 2006). and Martin Vaz hold the most isolated intertidal habitats One hundred and 25 reef fish species are known to within the Brazilian Province. Trindade was formed occur at Trindade Island and Martin Vaz Archipelago approximately 3.7 Mya (Cordani 1970) and is presently (154 fish species in total; Simon et al. 2013). The surrounded by calcareous algal reefs throughout the presence of a series of seamounts between Trindade- littoral zone (Gasparini and Floeter 2001). The tidepool Martin Vaz and the mainland (i.e., the Vitória-Trindade substrate is mostly basaltic, but tidepools near the lower- Chain), has been pointed out as serving as stepping- tide level have a higher proportion of biogenic carbon- stones (Kimura 1953) for reef fish species with reduced ate. During sampling, the mean water level relative to dispersal capabilities (Floeter and Gasparini 2000; the zero reference datum of Brazilian marine charts was Floeter et al. 2008). However, the recent discovery of 0.62 m and tide level ranged from −0.2 to 1.5 m. new species at the islands increased the endemism level from 5.7 % (Floeter et al. 2008) to 9.6 % (12 species; Tidepool characterization Simon et al. 2013). A large portion of the endemics (five) appear restricted to depths shallower than 20 m, Thirty-four tidepools unconnected to the sea or other which led Simon and colleagues (2013) to suggest that tidepools during the ebb tide were selected and evaluated these species have used the seamounts as stepping- for height, surface area, volume, depth, substrate rugos- stones during the Pleistocene lowstands. In these pe- ity, algal turf cover [the epilithic algal matrix sensu riods the sea level was as much as 130 m below present Wilson et al. (2003)], and substrate composition. The sea-level (Lambeck et al. 2002;Thomasetal.2009), and height of each tidepool was estimated as the vertical all seamounts were emerged, providing shallow habitats distance between tidepool water surface and sea level. to be colonized between Trindade and the mainland at Depth was measured with a ruler at haphazard points. distances shorter than 250 km. However, with rising sea The other substrate variables were estimated according to level, the shallow zone was eliminated from the Vitória- Macieira and Joyeux (2011). Water temperature and Trindade Chain. Species with limited dispersal capabil- salinity were measured with a mercury thermometer ities and restricted to these shallow habitats then became (0.5 ° C precision) and a refractometer (1 psu precision). isolated on the remaining easternmost islands, permit- ting allopatric speciation to occur. Such stepping-stones Sampling and sample processing and isolation processes linked to sea-level fluctuations are expected to be exacerbated for resident tidepool Sampling was conducted between October and organisms that would, therefore, be excellent models December 2009; fishes were fixed in 10 % formalin to infer such mechanisms. In the present work, the and later preserved in 70 % ethyl alcohol. The fishes community composition and structure of tidepool fishes were identified to the lowest possible taxonomic level, at Trindade were examined to detect if endemicity, measured (total length; TL, 0.1 mm) and weighed residency and number of individuals and mass appear (0.01 g). Species were categorized according to their linked. This would support the hypothesis degree of residency in tidepool habitats following Author's personal copy Environ Biol Fish (2015) 98:385–393 387 Fig. 1 Geographic position of the Vitória-Trindade Chain in the depths shallower than 200 m. The position of the Fernando de southwestern Atlantic (area delimited by larger rectangle) and
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